Smith combined his playing duties while on loan at Brechin City with managing the Dundee U-19 side before taking on the role of first team manager following the departure of previous manager Gordon Chisholm who was made redundant when the club went into administration in October 2010. Already admitted into Dundee's Hall of Fame[2] for making 400 appearances, scoring three goals and captaining the side from 1997 until 2006, Smith's status as a club legend[2] was cemented when he led the team to a club record 23-game unbeaten streak in the league.

Smith never gained a regular place at Celtic Park and joined fellow Scottish side Dundee in August 1995. He quickly established himself in the team at right-back and was made club captain in 1997, the same year Dundee achieved promotion to the Premier Division. After playing with the Dens Park side for ten-and-a-half seasons, Smith reached his testimonial year. He also took on the role of joint caretaker manager (with Bobby Mann) for the final two games of the 2005–2006 season following the dismissal of Alan Kernaghan.

At the end of the 2005–2006 season, Smith transferred to Icelandic outfit Valur, helping them to third place (in 2006) and winning (in 2007) the Icelandic Premier Division, their first championship in 20 years.

During the Icelandic close season, Smith was loaned back to Scottish clubs. In January 2007, he joined Partick Thistle, making 18 appearances and scoring one goal, while in January 2008 he joined Greenock Morton, making 5 appearances until he underwent a cartilage operation which kept him out for the rest of the season.

On 4 November 2008, Smith returned to Dundee as U19 coach, with his registration as a player following in January,[3] whereupon he was loaned out to neighbours Brechin City, with the ability to be recalled at any time. Brechin City's status as a part-time team enabled Smith to continue in his role as U19 Coach at Dens Park.[4]

On 15 October 2010, Smith was appointed manager of Dundee. He succeeded Gordon Chisholm, who had been made redundant after the club entered administration. Smith led the team to a club record unbeaten league streak of 23 games, guiding Dundee to safety despite the team receiving a 25-point deduction for entering administration for the second time in seven years (confirmed after a 0–1 win away to Ross County). This was rewarded, on 10 May 2011, when Smith signed a new three-year deal at Dundee, contracting him as manager until the end of the 2013–14 season.

On 1 July 2013, Smith joined Ross County as the club's Under-20s coach.[8] In January 2014, Smith was appointed manager of Scottish Championship club Alloa Athletic.[9] He guided Alloa to the final of the 2014–15 Scottish Challenge Cup.[10] Alloa defeated Rangers in the semi-final, with Smith noting the fact he had become the first Alloa manager to win a match against Rangers.[10] Smith said in December 2014 that he hoped to return to a full-time management job.[11] After a run of one win in 13 matches, he resigned as Alloa manager in March 2015.[11]